Liu Zuyao, Herbert Amy L, Chan Yingguang Frank, Kučka Marek, Kingsley David M, Peichel Catherine L
Division of Evolutionary Ecology, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.
Department of Developmental Biology, Stanford University School of Medicine, Stanford, California, United States of America.
PLoS Genet. 2025 May 9;21(5):e1011465. doi: 10.1371/journal.pgen.1011465. eCollection 2025 May.
Teleost fish are well-known for possessing a diversity of sex chromosomes and for undergoing frequent turnovers of these sex chromosomes. However, previous studies have mainly focused on variation between species, while comparatively little attention has been given to sex chromosome polymorphisms within species, which may capture early stages of sex chromosome changes. To better understand the evolution of sex chromosomes, we used the fourspine stickleback (Apeltes quadracus) as a model organism. Previous cytogenetic studies suggested that females of this species possessed a ZW heteromorphic sex chromosome system. However, genetic crosses and our whole-genome sequencing of three geographically distinct wild populations revealed that A. quadracus has an XY sex chromosome on chromosome 23. This chromosome has not previously been identified as a sex chromosome in any other stickleback species, indicating a recent sex chromosome turnover. We also identified two genes - rxfp2a and zar1l - as novel candidate sex determination genes. Notably, we observed inversions on both the X and Y chromosomes in different populations, resulting in distinctive patterns of differentiation between the X and Y chromosomes across populations. The new sex chromosome and intraspecies inversion polymorphisms observed in A. quadracus provide an excellent system for future work assessing the relative fitness effects of the inversions, which will enable testing theoretical models about the drivers of sex chromosome evolution and turnover.
硬骨鱼以拥有多样的性染色体以及这些性染色体的频繁更替而闻名。然而，以往的研究主要集中在物种间的变异，而对物种内性染色体多态性的关注相对较少，而这种多态性可能反映了性染色体变化的早期阶段。为了更好地理解性染色体的进化，我们以四棘刺鱼（Apeltes quadracus）作为模式生物。以往的细胞遗传学研究表明，该物种的雌性拥有ZW异型性染色体系统。然而，遗传杂交以及我们对三个地理上不同的野生种群进行的全基因组测序显示，四棘刺鱼在23号染色体上有一条XY性染色体。这条染色体在其他任何刺鱼物种中都未曾被鉴定为性染色体，这表明最近发生了性染色体更替。我们还鉴定出两个基因——rxfp2a和zar1l——作为新的候选性别决定基因。值得注意的是，我们在不同种群的X和Y染色体上都观察到了倒位，导致不同种群间X和Y染色体出现了独特的分化模式。在四棘刺鱼中观察到的新性染色体和种内倒位多态性为未来评估倒位相对适合度效应的研究提供了一个绝佳的系统，这将有助于检验关于性染色体进化和更替驱动因素的理论模型。
